Evolution and plasticity: Divergence of song discrimination is faster in birds with innate song than in song learners in Neotropical passerine birds

Plasticity is often thought to accelerate trait evolution and speciation. For example, plasticity in birdsong may partially explain why clades of song learners are more diverse than related clades with innate song. This “song learning” hypothesis predicts that (1) differences in song traits evolve faster in song learners, and (2) behavioral discrimination against allopatric song (a proxy for premating reproductive isolation) evolves faster in song learners. We tested these predictions by analyzing acoustic traits and conducting playback experiments in allopatric Central American sister pairs of song learning oscines (N = 42) and nonlearning suboscines (N = 27). We found that nonlearners evolved mean acoustic differences slightly faster than did leaners, and that the mean evolutionary rate of song discrimination was 4.3 times faster in nonlearners than in learners. These unexpected results may be a consequence of significantly greater variability in song traits in song learners (by 54–79%) that requires song‐learning oscines to evolve greater absolute differences in song before achieving the same level of behavioral song discrimination as nonlearning suboscines. This points to “a downside of learning” for the evolution of species discrimination, and represents an important example of plasticity reducing the rate of evolution and diversification by increasing variability.     

Urban noise influences vocalization structure in the House Wren Troglodytes aedon

Urban habitats are noisy and constrain acoustic communication in birds. We analysed the effect of anthropogenic noise on the vocalization characteristics of House Wrens Troglodytes aedon at two sites with different noise levels (rural and urban). We measured in each song and song trill the frequency bandwidth, maximum amplitude, highest and minimum frequency, and trill rate. In noisy urban environments, there was a reduction in bandwidth and an increase in trill rate relative to quieter, rural environments. The whole song of birds from both populations increased in minimum frequency as noise increased, improving song transmission.     

Different frequency control mechanisms and the exploitation of frequency space in passerines

1. Birdsong is used in reproductive context and, consequently, has been shaped by strong natural and sexual selection. The acoustic performance includes a multitude of acoustic and temporal characteristics that are thought to honestly reveal the quality of the singing individual.
2. One major song feature is frequency and its modulation. Sound frequency can be actively controlled, but the control mechanisms differ between different groups. Two described mechanisms are pressure‐driven frequency changes in suboscines and control by syringeal muscles in oscines.
3. To test to what degree these different control mechanisms enhance or limit the exploitation of frequency space by individual species and families, we compared the use of frequency space by tyrannid suboscines and emberizid/passerellid oscines.
4. We find that despite the different control mechanisms, the songs of species in both groups can contain broad frequency ranges and rapid and sustained frequency modulation (FM). The maximal values for these parameters are slightly higher in oscines.
5. Furthermore, the mean frequency range of song syllables is substantially larger in oscines than suboscines. Species within each family group collectively exploit equally broadly the available frequency space.
6. The narrower individual frequency ranges of suboscines likely indicate morphological specialization for particular frequencies, whereas muscular control of frequency facilitated broader exploitation of frequency space by individual oscine species.

     

A latitudinal gradient in rates of evolution of avian syllable diversity and song length

We ask whether rates of evolution in traits important for reproductive isolation vary across a latitudinal gradient, by quantifying evolutionary rates of two traits important for pre-mating isolation-avian syllable diversity and song length. We analyse over 2500 songs from 116 pairs of closely related New World passerine bird taxa to show that evolutionary rates for the two main groups of passerines-oscines and suboscines-doubled with latitude in both groups for song length. For syllable diversity, oscines (who transmit song culturally) evolved more than 20 times faster at high latitudes than in low latitudes, whereas suboscines (whose songs are innate in most species and who possess very simple song with few syllable types) show no clear latitudinal gradient in rate. Evolutionary rates in oscines and suboscines were similar at tropical latitudes for syllable complexity as well as for song length. These results suggest that evolutionary rates in traits important to reproductive isolation and speciation are influenced by latitude and have been fastest, not in the tropics where species diversity is highest, but towards the poles.     

Neighbor-stranger discrimination by song in a suboscine bird, the alder flycatcher, Empidonax alnorum

Bird song and its functions have been studied extensively formore than 50 years, but almost entirely in oscine passerines.Few studies have investigated any aspect of song in suboscinepasserines. This is significant because song development andthe extent of individual variation in song differs greatly betweenthese groups. Learning and auditory feedback play major rolesin song development in all oscines studied, but apparently nopart in song ontogeny in suboscines. The ability of territorialoscine males to discriminate between songs of neighbors andstrangers has received considerable attention, but this phenomenonis virtually unstudied in suboscines. We tested whether a suboscinebird, the alder flycatcher (Empidonax alnorum), was able todiscriminate between songs of neighbors and strangers despitelimited individual variation in song. We performed playbackexperiments to measure responses of males to songs of neighborsand strangers broadcast from the territory boundary shared bythe subject and the neighbor. Subjects responded more aggressivelyto songs of strangers than to songs of neighbors. These resultsfurther our understanding of the evolution of song and its functionsin suboscines by demonstrating that, similar to their oscinerelatives, they can discriminate between the songs of neighborsand strangers.     

Signalling through acoustic windows: nightingales avoid interspecific competition by short-term adjustment of song timing

The function of bird song is closely linked to sexual selection through female choice and male–male competition, and thus variation in communication success is likely to have major fitness consequences for a singing male. A crucial constraint on signal transmission is imposed by background noise, which may include songs from other species. I investigated whether singing nightingales (Luscinia megarhynchos) avoid temporal overlap with the songs of other bird species in a playback experiment. I analysed the temporal song patterns of six males, each of which were exposed to songs of other species. The nightingales significantly avoided overlapping their songs with the playback songs, and started singing preferentially during the silent intervals between the heterospecific songs. This timing of song onset produced a greater variability in pause duration compared to the nightingales’ undisturbed solo singing. These findings suggest that birds adjust their song timing to avoid acoustic interference on short temporal scales, and thus are able to improve the efficiency of acoustic communication in complex sonic environments. Moreover, the results indicate that temporal song patterns can be affected by the songs of other species, and thus such influences should be taken into account when studying bird song in the field.     

Different behavioural responses to anthropogenic noise by two closely related passerine birds

Anthropogenic noise, now common to many landscapes, can impair acoustic communication for many species, yet some birds compensate for masking by noise by altering their songs. The phylogenetic distribution of these noise-dependent signal adjustments is uncertain, and it is not known whether closely related species respond similarly to noise. Here, we investigated the influence of noise on habitat occupancy rates and vocal frequency in two congeneric vireos with similar song features. Noise exposure did not influence occupancy rates for either species, yet song features of both changed, albeit in different ways. With increases in noise levels, plumbeous vireos (Vireo plumbeus) sang shorter songs with higher minimum frequencies. By contrast, grey vireos (Vireo vicinior) sang longer songs with higher maximum frequencies. These findings support the notion that vocal plasticity may help some species occupy noisy areas, but because there were no commonalities among the signal changes exhibited by these closely related birds, it may be difficult to predict how diverse species may modify their signals in an increasingly noisy world.     

Bird song and anthropogenic noise: vocal constraints may explain why birds sing higher-frequency songs in cities

When animals live in cities, they have to adjust their behaviour and life histories to novel environments. Noise pollution puts a severe constraint on vocal communication by interfering with the detection of acoustic signals. Recent studies show that city birds sing higher-frequency songs than their conspecifics in non-urban habitats. This has been interpreted as an adaptation to counteract masking by traffic noise. However, this notion is debated, for the observed frequency shifts seem to be less efficient at mitigating noise than singing louder, and it has been suggested that city birds might use particularly high-frequency song elements because they can be produced at higher amplitudes. Here, we present the first phonetogram for a songbird, which shows that frequency and amplitude are strongly positively correlated in the common blackbird (Turdus merula), a successful urban colonizer. Moreover, city blackbirds preferentially sang higher-frequency elements that can be produced at higher intensities and, at the same time, happen to be less masked in low-frequency traffic noise.     

Global macroevolution and macroecology of passerine song

Studying the macroevolution of the songs of Passeriformes (perching birds) has proved challenging. The complexity of the task stems not just from the macroevolutionary and macroecological challenge of modeling so many species, but also from the difficulty in collecting and quantifying birdsong itself. Using machine learning techniques, we extracted songs from a large citizen science dataset, and then analyzed the evolution, and biotic and abiotic predictors of variation in birdsong across 578 passerine species. Contrary to expectations, we found few links between life‐history traits (monogamy and sexual dimorphism) and the evolution of song pitch (peak frequency) or song complexity (standard deviation of frequency). However, we found significant support for morphological constraints on birdsong, as reflected in a negative correlation between bird size and song pitch. We also found that broad‐scale biogeographical and climate factors such as net primary productivity, temperature, and regional species richness were significantly associated with both the evolution and present‐day distribution of bird song features. Our analysis integrates comparative and spatial modeling with newly developed data cleaning and curation tools, and suggests that evolutionary history, morphology, and present‐day ecological processes shape the distribution of song diversity in these charismatic and important birds.     

Changes in adult zebra finch song require a forebrain nucleus that is not necessary for song production

Male zebra finches normally crystallize song at approximately 90 days and do not show vocal plasticity as adults. However, changes to adult song do occur after unilateral tracheosyringeal (ts) nerve injury, which denervates one side of the vocal organ. We examined the effect of placing bilateral lesions in LMAN (a nucleus required for song development but not for song maintenance in adults) upon the song plasticity that is induced by ts nerve injury in adults. The songs of birds that received bilateral lesions within LMAN followed by right ts nerve injury silenced, on average, 0.25 syllables, and added 0.125 syllables (for an average turnover of 0.375 syllables), and changed neither the frequency with which individual syllables occurred within songs nor the motif types they used most often. In contrast, the songs of birds that received sham lesions followed by ts nerve injury lost, on average, 1.625 syllables, silenced 0.125 syllables, and added 0.75 syllables, turning over an average of 2.5 syllables. They also significantly changed both the frequency with which individual syllables were included in songs and the motif variants used. Thus, song plasticity induced in adult zebra finches with crystallized songs requires the presence of LMAN, a nucleus which had been thought to play a role in vocal production only during song learning. Although the changes to adult songs induced by nerve transection are more limited than those that arise during song development, the same circuitry appears to underlie both types of plasticity.     

Anthropogenic noise decreases urban songbird diversity and may contribute to homogenization

More humans reside in urban areas than at any other time in history. Protected urban green spaces and transportation greenbelts support many species, but diversity in these areas is generally lower than in undeveloped landscapes. Habitat degradation and fragmentation contribute to lowered diversity and urban homogenization, but less is known about the role of anthropogenic noise. Songbirds are especially vulnerable to anthropogenic noise because they rely on acoustic signals for communication. Recent studies suggest that anthropogenic noise reduces the density and reproductive success of some bird species, but that species which vocalize at frequencies above those of anthropogenic noise are more likely to inhabit noisy areas. We hypothesize that anthropogenic noise is contributing to declines in urban diversity by reducing the abundance of select species in noisy areas, and that species with low‐frequency songs are those most likely to be affected. To examine this relationship, we calculated the noise‐associated change in overall species richness and in abundance for seven common songbird species. After accounting for variance due to vegetative differences, species richness and the abundance of three of seven species were reduced in noisier locations. Acoustic analysis revealed that minimum song frequency was highly predictive of a species' response to noise, with lower minimum song frequencies incurring greater noise‐associated reduction in abundance. These results suggest that anthropogenic noise affects some species independently of vegetative conditions, exacerbating the exclusion of some songbird species in otherwise suitable habitat. Minimum song frequency may provide a useful metric to predict how particular species will be affected by noise. In sum, mitigation of noise may enhance habitat suitability for many songbird species, especially for species with songs that include low‐frequency elements.     

Effects of urban noise on song and response behaviour in great tits

Acoustic communication is fundamental in avian territory defence and mate attraction. In urban environments where sound transmissions are more likely to be masked by low-frequency anthropogenic noise, acoustic adaptations may be advantageous. However, minor modifications to a signal could affect its efficacy. While recent research has shown that there is divergence between songs from noisy and quiet areas, it is unknown whether these differences affect the response to the signal by its receivers. Here, we show that there is a difference in spectral aspects of rural and urban song in a common passerine, the great tit Parus major, at 20 sites across the UK. We also provide, to our knowledge, the first demonstration that such environmentally induced differences in song influence the response of male territory holders. Males from quiet territories exhibited a significantly stronger response when hearing song from another territory holder with low background noise than from those with high background noise. The opposite distinction in response intensity to homotypic versus heterotypic song was observed in males from noisy territories. This behavioural difference may intensify further signal divergence between urban and rural populations and raises important questions concerning signal evolution.     

Differences in Frequency of Shared Song Types Enables Neighbour‐Stranger Discrimination in a Songbird Species with Small Song Repertoire

Acoustic Neighbour‐Stranger (N‐S) discrimination is widespread in birds and has evolved to settle territorial disputes with low costs. N‐S discrimination was found both in song‐learning oscines and non‐song‐learning bird taxa, irrespective of the repertoire sizes they have. Therefore, it seems that more than just a single mechanism enable N‐S discrimination. Species with larger repertoires, where males have unique phrases or syllables may rely on such interindividual differences. The majority of birds have rather small repertoires, which often are shared among neighbours. In this case, males are facing the problem of individual recognition when rivals produce songs, at least superficially, identical. To better understand the acoustic basis of N‐S discrimination in species with small and shared repertoires, I studied the ortolan bunting (Emberiza hortulana). Males of this small oscine species are able to N‐S discrimination based on a single song rendition when presented in a playback experiment, regardless of song‐type diversity and song‐sharing level within a particular population. It was also found that songs of the same type sung by different males differ in the frequency of the initial song phrases and these differences persist over years. Here, I tested whether males are able to discriminate among the natural songs and the artificially modified songs of their neighbours in which the frequency was experimentally changed by relatively small value in comparison with the variation range found in this population. Subjects responded significantly more aggressively to the songs with an artificially modified frequency, suggesting that males treat such songs as having come from the repertoire of a non‐neighbour. These results confirm an earlier prediction that differences in the frequency of shared song types enable N‐S discrimination. The study presents one of the possible mechanisms enabling N‐S discrimination in songbirds with small repertoires and stress the role of within‐song‐type variation, which is still understudied song characteristic.     

House Wrens Troglodytes aedon reduce repertoire size and change song element frequencies in response to anthropogenic noise

Anthropogenic noise (≤ 3 kHz) can affect key features of birds’ acoustic communication via two different processes: (1) song‐learning, because songbirds need to hear themselves and other birds to crystallize their song, and (2) avoidance of song elements that overlap with anthropogenic noise. In this study we tested whether anthropogenic noise reduces the number of song elements in the repertoire of House Wren Troglodytes aedon, an urban species. Additionally, we tested whether the proportion of high‐frequency elements (i.e. elements where the minimum frequency is above 3 kHz) is related to anthropogenic noise levels, and how the frequencies and duration of shared elements between males change with different levels of anthropogenic noise. We recorded 29 House Wren males exposed to different anthropogenic noise levels (36.50–79.50 dB) during two consecutive breeding seasons from four locations. We recorded each male on 2 days during each season continuously for 50 min (we collected 104 h of recordings) and measured anthropogenic noise levels every 10 min inside each male territory during the recording period. In general, individuals inhabiting noisier territories had smaller repertoires. However, only in two locations with anthropogenic noise levels between 38.60 and 79.50 dB did males inhabiting noisier territories have smaller repertoires. In the other two locations with lower anthropogenic noise (36.50–66.50 dB), the anthropogenic noise inside each territory was not related to the repertoire size. Individuals inhabiting the noisiest location showed a tendency to include more high‐frequency elements in their songs. In 26% of the elements, the anthropogenic noise affected their frequency features. Our results showed that not all House Wrens inhabiting urban environments modify their songs at the highest level of organization (i.e. repertoire) to reduce the masking effect of anthropogenic noise on acoustic communication.     

Community convergence in bird song

Species in similar habitats are often similar in morphology or behaviour, attributed to adaptation to similar environmental selection pressures, sometimes mediated by competitive interactions. For passerine songs, similarity of phenotype in identical habitats and character displacement have been documented, the former due to adaptation to the acoustics of the habitat, and the latter due to competition for acoustic space among species. If these phenomena are widespread, they should lead to community convergence of bird songs. Here, we test if passerine communities in similar habitats converge in song attributes or in acoustic differentiation among species. We compared the songs of European and North American Mediterranean climate passerine communities in open and closed habitats. Song frequency varied across different habitats but not continents. This was independent of both phylogeny and body size, indicating community convergence due to acoustic adaptation, rather than species sorting or similarity as a by-product of another type of ecological convergence. We found little evidence for regular spacing in song features among species, as would be expected if acoustic competition shapes within-community structure. However, for one of five song components, the open habitat communities showed a similar distribution of phenotypes on each continent. The proportion of interspecific variation in song explained by these effects was small. The fact that songs are complex signals that vary in many dimensions may explain why competition for acoustic space seems to be of small importance in structuring songs in these passerine communities.     

Perineuronal nets and vocal plasticity in songbirds: A proposed mechanism to explain the difference between closed‐ended and open‐ended learning

Perineuronal nets (PNN) are aggregations of chondroitin sulfate proteoglycans surrounding the soma and proximal processes of neurons, mostly GABAergic interneurons expressing parvalbumin. They limit the plasticity of their afferent synaptic connections. In zebra finches PNN develop in an experience‐dependent manner in the song control nuclei HVC and RA (nucleus robustus arcopallialis) when young birds crystallize their song. Because songbird species that are open‐ended learners tend to recapitulate each year the different phases of song learning until their song crystallizes at the beginning of the breeding season, we tested whether seasonal changes in PNN expression would be found in the song control nuclei of a seasonally breeding species such as the European starling. Only minimal changes in PNN densities and total number of cells surrounded by PNN were detected. However, comparison of the density of PNN and of PNN surrounding parvalbumin‐positive cells revealed that these structures are far less numerous in starlings that show extensive adult vocal plasticity, including learning of new songs throughout the year, than in the closed‐ended learner zebra finches. Canaries that also display some vocal plasticity across season but were never formally shown to learn new songs in adulthood were intermediate in this respect. Together these data suggest that establishment of PNN around parvalbumin‐positive neurons in song control nuclei has diverged during evolution to control the different learning capacities observed in songbird species. This differential expression of PNN in different songbird species could represent a key cellular mechanism mediating species variation between closed‐ended and open‐ended learning strategies. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 975–994, 2017     

Conveying information with one song type: changes in dawn song performance correspond to different female breeding stages

Many bird species participate in dawn singing, a behaviour categorized by intensive singing at dawn; however, many of these species deliver only one song type at dawn. While there are many proximate and ultimate hypotheses for why birds sing at dawn, little is known about whether males are able to vary one simple song to convey different information. We used autonomous acoustic recorders to record dawn songs of field sparrows and quantified three parameters of singing performance: 1) bout length, 2) song rate, and 3) song complexity. We found that males sang the longest dawn bouts during their mate's fertile period, the highest song rates during the post-fertile period, and the most complex songs during the pre-fertile period. The change in dawn singing behaviour with their mate's breeding stage suggest the purpose of dawn song may be context dependent. Our results demonstrate that male field sparrows, while only having a single song type sung at dawn, may convey information for both intra- and intersexual purposes. While it is generally assumed that dawn song has a specific function, the variability in the duration, rate, and complexity of dawn song in field sparrows suggests that they are conveying different information and that dawn song likely has multiple functions.     

Body size correlates negatively with the frequency of distress calls and songs of Neotropical birds

ABSTRACT The allometric relationship between body size and song frequency has been established in previous studies of temperate and tropical bird communities. However, the relationship between body size and the frequency of distress calls has been examined in only one study of temperate birds. We examined size‐frequency relationships in the distress calls and songs of a Neotropical bird community in northwestern Costa Rica. In 2008 and 2009, we recorded distress calls and determined the body mass of 54 mist‐netted birds representing 38 species, 35 genera, and 14 families. We obtained songs for these same species from sound libraries and commercially available compact discs. For each vocalization, we measured minimum frequency and frequency of maximum amplitude. Larger birds produced lower‐frequency distress calls and songs than smaller birds. Phylogenetically controlled analyses revealed that the frequency of maximum amplitude was negatively correlated with body mass for both distress calls and songs. Minimum frequency was negatively correlated with mass for distress calls, but not songs. Our analyses suggest that the influence of phylogeny on the relationship between frequency characteristics and body size is modest. Pair‐wise comparisons across 37 species revealed that distress calls and songs had similar minimum frequencies, but songs had significantly lower frequencies of maximum amplitude than distress calls. This difference may arise from differences in signal function. Lower‐frequency sounds should transmit farther through forest habitats and songs must often transmit longer distances to reach their intended audience than distress calls. Our results support the general theory that body size is negatively correlated with the frequency of acoustic signals by demonstrating that this pattern holds true for both distress calls and songs in a Neotropical bird community.     

Song divergence at the edge of Amazonia: an empirical test of the peripatric speciation model

The evolutionary divergence of mating signals provides a powerful basis for animal speciation. Divergence in sympatry strengthens reproductive isolation, and divergence in allopatry can reduce or eliminate gene flow between populations on secondary contact. In birds, the first of these processes has empirical support, but the second remains largely hypothetical. This is perhaps because most studies have focused on oscine passerines, whose song learning ability may reduce the influence of vocalizations in reproductive isolation. In suboscine passerines, the role of learning in song development is thought to be minimal, and the resultant signals are relatively fixed. To investigate the role of song in the early stages of peripatric speciation, we therefore studied a suboscine, the chestnut‐tailed antbird Myrmeciza hemimelaena. We recorded male songs in a natural forest island (isolated for < 3000 years) at the southern fringe of Amazonia, and at two nearby sites in continuous forest. A previous study found the isolated population to be weakly differentiated genetically from the ancestral population suggesting that peripatric speciation was underway. In support of this, although we detected minor but significant differences in song structure between each site, the most divergent songs were those of island birds. On simulating secondary contact using playback, we found that pairs from the forest island responded more strongly to island (i.e. local) songs than to those from both non‐island sites, and vice versa. This pattern was not observed in pairs from one non‐island site, which responded with equal strength to local songs and songs from the other non‐island site. Island females were more likely to approach and sing after hearing local male songs, rather than songs from the non‐island populations, and vice versa; non‐island females did not appear to discriminate between local songs and those from the other non‐island site. These findings are consistent with the idea that vocal divergence arising in small populations at the edge of Amazonia may result in partial reproductive isolation when contact is resumed. They also suggest the possibility that song divergence in peripatry may, after much longer time‐frames, act as a barrier to gene flow in suboscines, perhaps because of an inability to learn or recognize divergent songs on secondary contact. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90 , 173–188.     

Geographical variation in the vocalizations of the suboscine Thorn‐tailed Rayadito Aphrastura spinicauda

Structural variation in acoustic signals may be related either to the factors affecting sound production such as bird morphology, or to vocal adaptations to improve sound transmission in different environments. Thus, variation in acoustic signals can influence intraspecific communication processes. This will ultimately influence divergence in allopatric populations. The study of geographical variation in vocalizations of suboscines provides an opportunity to compare acoustic signals from different populations, without additional biases caused by song learning and cultural evolution typical of oscines. The aim of this study was to compare vocalizations of distinct populations of a suboscine species, the Thorn‐tailed Rayadito. Four types of vocalizations were recorded in five populations, including all three currently accepted subspecies. Comparisons of each type of vocalization among the five populations showed that some variation existed in the repetitive trill, whereas no differences were found among alarm calls and loud trills. Variation in repetitive trills among populations and forest types suggests that sound transmission is involved in vocal differences in suboscines. Acoustic differences are also consistent with distinguishing subspecies bullocki from spinicauda and fulva, but not the two latter subspecies from each other. Our results suggest that the geographical differentiation in vocalizations observed among Thorn‐tailed Rayadito populations is likely to be a consequence of different ecological pressures. Therefore, incipient genetic isolation of these populations is suggested, based on the innate origin of suboscine vocalizations.